Does the Vulnerable sun bear Helarctos malayanus damage crops and threaten people in oil palm plantations?
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Does the Vulnerable sun bear Helarctos malayanus
damage crops and threaten people in oil palm
plantations?
ROSHAN GUHARAJAN, NICOLA K. ABRAM, MOHD AZZUMAR MAGGUNA
B E N O Î T G O O S S E N S , S I E W T E W O N G , S E N T H I L V E L K . S . S . N A T H A N and
DAVID L. GARSHELIS
Abstract Largely as a result of the expansion of oil palm nutritional benefit from oil palm, plantations do not provide
Elaeis guineensis, forest fragmentation has occurred on a the diversity of food and cover available in a natural forest.
large scale in Borneo. There is much concern about how for-
Keywords Borneo, crop damage, Helarctos malayanus,
est-dependent species, such as the Vulnerable sun bear
human–wildlife conflict, Lower Kinabatangan, mortality
Helarctos malayanus, can persist in this landscape. The ab-
risk, oil palm, Sabah
sence of sufficient natural food in forest fragments could
drive sun bears into oil palm plantations, where they risk Supplementary material for this article can be found at
coming into conflict with people. We interviewed oil palm https://doi.org/./S
plantation workers and farmers in the Lower Kinabatangan
region of Sabah, Malaysian Borneo, to ascertain if sun bears
were utilizing plantations, if they were causing damage to
the crop, and how the bears were perceived by people. To Introduction
obtain a comparative baseline we extended these questions
to include other species as well. We found that bears were
rarely encountered in plantations and were not considered
to be destructive to the oil palm crop, although they were
M alaysia is the second largest grower of oil palm Elaeis
guineensis (U.S. Department of Agriculture, Foreign
Agricultural Service, ). However, the expansion of the
generally feared. Other species, such as macaques Macaca industry has had serious implications: during –,
spp., bearded pigs Sus barbatus, and elephants Elephas max- –% of Malaysian oil palm plantations were established
imus, had more destructive feeding habits. Sun bears could through forest conversion (Koh & Wilcove, ), and oil
use this readily available food resource without being tar- palm agriculture has adverse impacts on biodiversity (Yue
geted for retribution, although incidental human-related et al., ; Vijay et al., ). Wildlife that enter plantations
mortality remains a risk. Although bears could gain some are at risk of being hunted, or subject to retribution for dam-
aging crops (Meijaard et al., ; Azhar et al., ; Luskin
et al., ). Oil palm plantations can be nutritionally poor
for some species, such as orang-utans Pongo spp.
ROSHAN GUHARAJAN* (Corresponding author) and DAVID L. GARSHELIS† (Campbell-Smith et al., ), whereas others utilize the
Department of Fisheries, Wildlife and Conservation Biology, University of
Minnesota, 135 Skok Hall, 2003 Upper Buford Circle, St. Paul, Minnesota abundance of palm fruits and rodents as prey (Rajaratnam
55108, USA. E-mail roshang88@gmail.com et al., ; Nakashima et al., ). Certain species can use
NICOLA K. ABRAM Living Landscape Alliance, Kota Kinabalu, Sabah, Malaysia; oil palm landscapes as corridors (Campbell-Smith et al.,
and ARC Centre of Excellence for Environmental Decisions, University of ; Estes et al., ) and feeding and resting sites
Queensland, Brisbane, Australia and Forever Sabah, Kota Kinabalu, Sabah,
Malaysia (Nakashima et al., ; Ancrenaz et al., ).
MOHD AZZUMAR MAGGUNA and BENOÎT GOOSSENS‡ Danau Girang Field Centre,
Borneo is a stronghold for the sun bear Helarctos malaya-
Kota Kinabalu, Sabah, Malaysia nus (Augeri, ), which is categorized as Vulnerable on
SIEW TE WONG Bornean Sun Bear Conservation Centre, Sandakan, Sabah, the IUCN Red List (Fredriksson et al., ). Previous re-
Malaysia search on Borneo showed that sun bears are sensitive to ex-
SENTHILVEL K.S.S. NATHAN Sabah Wildlife Department, Kota Kinabalu, Sabah, treme variation in supra-annual mast fruiting events, with
Malaysia some bears starving during long inter-mast periods (Wong
*Current address: Leibniz Institute for Zoo and Wildlife Research, Alfred- et al., ; Fredriksson et al., ) and others using crop-
Kowalke-Str. 17, 10315 Berlin, Germany
†Also at: Minnesota Department of Natural Resources, Grand Rapids, lands to supplement their diet (Fredriksson, ; Cheah,
Minnesota, USA ). With oil palm plantations now bordering many forests
‡Also at: School of Biosciences, Cardiff University, Cardiff, UK; Sustainable in Borneo, this crop could, to some degree, be a potential
Places Research Institute, Cardiff University, Cardiff, UK; and Sabah Wildlife
Department, Kota Kinabalu, Sabah, Malaysia supplementary food source for bears, especially during
Received January . Revision requested March . periods of low natural food availability. However, increased
Accepted June . First published online December . reliance on agricultural products for food often comes with
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
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https://doi.org/10.1017/S0030605317001089
612 R. Guharajan et al.
the risk of conflict and persecution (Fredriksson, ; Liu on them. We asked respondents to rate how often they
et al., ; Scotson et al., ). saw specific species (rarely or commonly; we did not provide
Interview surveys have been used successfully to gauge guidance on these terms), where they saw them (within
perceptions and attitudes towards wildlife in oil palm plan- plantation, plantation–forest border, and/or secondary for-
tations (Azhar et al., ; Luskin et al., ; Ancrenaz et al., est within plantations) and at what time the encounter(s)
). We used interview surveys to understand the use of took place (morning, afternoon and/or night).
plantations by sun bears, whether their feeding damaged We asked whether the observed species fed on loose palm
crops, and whether people perceived them as a threat. We fruits that had fallen to the ground (hereafter loose fruits),
hypothesized that conversion of forest to oil palm would harvested fruit bunches on the ground (hereafter fruit
force sun bears to use this resource more, compounding re- bunches), fruits on the palms (hereafter palm fruits), and/
taliation against them. We collected information on mul- or oil palm shoots (hereafter palm shoots). We asked re-
tiple species for comparison with sun bears. spondents to identify species that were destructive (yes or
no) towards oil palms as a result of their feeding habits.
We also asked whether each species was considered to be
Study area dangerous (yes or no); if the respondent answered yes, we
asked them to rate this qualitatively (least dangerous, dan-
Our study area was the Lower Kinabatangan floodplain in
gerous, or extremely dangerous). We asked respondents to
Sabah, Malaysian Borneo (Fig. ). The original forest land-
provide details of their reaction to encounters with danger-
scape has been altered by logging and agriculture, beginning
ous species: did they retreat, chase the animal away, capture
in the s (Azmi, ), leaving degraded, fragmented for-
it and/or kill it? We ended each interview by asking respon-
est surrounded by oil palm. Most of the remaining forest
dents how they felt about hunting and protecting wildlife.
(c. , ha) lies within the Lower Kinabatangan Wildlife
These questions were asked towards the end to minimize
Sanctuary and several forest reserves. Forest types in the
any bias in reporting.
floodplain include mangrove forest, Nypa fruticans swamp,
freshwater swamp forest, peat swamp forest, and mixed dip-
terocarp forest (Abram et al., ). Besides the sun bear, Data analysis
prominent wildlife species include the Bornean orang-utan
We conducted all analyses in R .. (R Development Core
Pongo pygmaeus, the Bornean elephant Elephas maximus
Team, ). For examination of wildlife encounters we
borneensis and the Sunda clouded leopard Neofelis diardi.
grouped seven species into three groups: macaques (Macaca
fascicularis, M. nemestrina), snakes (Naja sumatrana, Python
Methods reticulatus, Python breitensteini), and civets (Viverra tanga-
lunga, Paradoxurus hermaphroditus). We excluded squirrels,
Data collection birds and monitor lizards from all summaries and analyses
regarding wildlife encounters. For the purpose of ranking we
We interviewed respondents from oil palm plantations calculated the mean commonness ( = rare, = common),
in June and during May–October , within a section destructiveness ( = yes, = no), and perceived danger level
of the Lower Kinabatangan (Fig. ). We sampled plantations ( = not dangerous, = least dangerous, = dangerous,
where we gained permission: oil palm estates (hereafter = extremely dangerous) of each species (Marchal & Hill,
estates) and small farms (known as kebun). In estates ). We did not include non-answers in these calculations
we interviewed the operations staff, whereas in kebun we because we assumed if respondents did not answer, it meant
spoke to the farmers themselves. We obtained information they had no opinion.
on the total planted area (hereafter plantation size), the We then separated all species into two groups based on
presence of immature and mature palms (mature . body size, as we predicted larger species might be perceived
years old), and whether the plantation bordered forest as being more destructive and dangerous, as well as more vis-
(hereafter border). We asked respondents their age (here- ible. One group included all large-bodied mammals (. kg;
after age) and how long they had worked in the plantation hereafter large mammals); the other group included smaller-
(hereafter time, in four categories: , year, – years, – bodied mammals and snakes (hereafter small wildlife). We
years, . years). summed the number of species in each group per
We asked respondents to identify wildlife encountered in respondent.
plantations (mammals and certain reptiles), using reference We fit Poisson generalized linear models with the total
images of protected species in Sabah (Sabah Wildlife count of small wildlife or large mammals encountered per
Department, ; WWF-Malaysia, ). We did not in- respondent as the response. We included the binary vari-
clude birds, squirrels or monitor lizards Varanus spp., but ables border, immature and mature palms, the categorical
recorded these when respondents provided information variable plantation type, and the continuous variable
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
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https://doi.org/10.1017/S0030605317001089Sun bears in oil palm plantations 613
FIG. 1 Locations of oil palm
plantations targeted for
interviews in the Lower
Kinabatangan, Sabah,
Malaysian Borneo.
plantation size as plantation-level predictors. We also in- for multicollinearity in the same way as for the Poisson gen-
cluded the categorical variable time and the continuous vari- eralized linear models. We assessed model fit by visually in-
able age as respondent-level predictors. We began by fitting specting binned residual versus fitted plots. We calculated
single covariate models and subsequently adding predictors area under the receiver operating characteristics curve to dis-
that were present in models with the lowest Akaike informa- cern model predictive power. We fit a binomial generalized
tion criterion corrected for small sample sizes (ΔAICc , ) linear mixed model to compare model coefficients and %
in each successive step. We selected top-ranked models confidence intervals with the generalized linear model.
based on AICc and model weights, ignoring competing
models with only one additional variable to a better ranked
model (Arnold, ). We checked all top-ranked models for Results
overdispersion by dividing model residual deviance by de-
grees of freedom. We assessed multicollinearity between Estates (n = , x mean area = , ± SD . ha) were
model predictors using generalized variance inflation factor much larger than kebun (n = , x mean area = ± SD . ha).
values. We judged model fit visually by plotting residuals Most plantations (.%) had only mature palms, .% had
against fitted values. As respondents from the same planta- only immature palms, and .% had a combination of both.
tion might have had correlated observations, we further fit Most respondents (.%) had worked in their plantation
Poisson generalized linear mixed models with plantation as for . years; .% had worked for – years, .% for
the random intercept. We compared the generalized linear – years, and .% for , year. Most respondents felt that
model and generalized linear mixed model coefficients and protecting wildlife was necessary (.%). Some (.%) felt
% confidence intervals. that they should be allowed to hunt, but a larger number
For all analyses regarding wildlife feeding habits we in- (.%) felt this was not necessary (the rest did not answer).
cluded observations of birds and squirrels, as the goal was More than half the respondents (.%) felt they should be
to understand food resource use and perceived destructive- allowed to keep wildlife as pets.
ness. We removed observations that solely involved second- Respondents encountered at least species (Table ).
hand information received by respondents about depreda- Most (%) encounters occurred within the oil palm planta-
tions. To model the effects of feeding behaviours and planta- tion, with another .% occurring at the border of forest
tion characteristics on destructiveness, we fit binomial and plantation, and .% in secondary forest patches.
generalized linear models with destructive behaviour as the Encounters often took place in the morning (.%), but
binary response variable, and the binary predictor variables also in the afternoon (%) and at night (.%).
loose fruits, fruit bunches, palm fruits, palm shoots, immature Respondents rarely encountered sun bears within planta-
and mature palms. We also included plantation type as a cat- tions (Table ). Sun bears were encountered somewhat
egorical predictor variable. We selected models and checked more commonly than clouded leopards and Sunda
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
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https://doi.org/10.1017/S0030605317001089614 R. Guharajan et al.
TABLE 1 Mean ± SD commonness ranks, with the total number of records of mammals and reptiles encountered by respondents (n = )
from oil palm plantations in the Lower Kinabatangan, Sabah, Malaysia (Fig. ), and the number of records in which respondents were able
to rank the species.
Mean ± SD Total no. No. of
Species commonness rank1 of records ranked records2
Sunda clouded leopard Neofelis diardi 1.00 ± 0.00 2 2
Sunda pangolin Manis javanica 1.05 ± 0.22 27 21
Muntjac Muntiacus sp. 1.09 ± 0.30 13 11
Sambar Rusa unicolor 1.17 ± 0.38 32 30
Sun bear Helarctos malayanus 1.25 ± 0.46 8 8
Porcupine Hystrix sp. 1.29 ± 0.46 40 38
Malay badger Mydaus javanensis 1.31 ± 0.47 29 29
Mousedeer Tragulus sp. 1.31 ± 0.48 16 16
Western tarsier Tarsius bancanus 1.33 ± 0.52 6 6
Bornean elephant Elephas maximus borneensis 1.33 ± 0.47 57 52
Bornean orang-utan Pongo pygmaeus 1.34 ± 0.48 52 50
Proboscis monkey Nasalis larvatus 1.38 ± 0.49 32 29
Slow loris Nycticebus sp. 1.40 ± 0.55 6 5
Müller’s Bornean gibbon Hylobates muelleri 1.47 ± 0.52 16 15
Smooth-coated otter Lutrogale perspicillata 1.48 ± 0.50 49 48
Snakes Python spp., Naja sumatrana 1.48 ± 0.50 133 125
Colugo Galeopterus variegatus 1.50 ± 0.71 2 2
Leopard cat Prionailurus bengalensis 1.58 ± 0.50 38 36
Civets Viverra tangalunga, Paradoxurus hermaphroditus 1.59 ± 0.50 84 80
Estuarine crocodile Crocodylus porosus 1.60 ± 0.52 11 10
Bearded pig Sus barbatus 1.77 ± 0.42 98 96
Macaque Macaca spp. 1.94 ± 0.23 151 144
Ranks: , rarely encountered; , commonly encountered.
This number was used in the calculation of the mean commonness rank.
pangolins Manis javanica, but less commonly than ele- said this was true of sun bears (Fig. ). Respondents identi-
phants and orang-utans. The most commonly reported spe- fied these feeding habits based on visual observations
cies were macaques, bearded pigs Sus barbatus, civets and (.%), feeding signs (.%) and information received
leopard cats Prionailurus bengalensis. from others (%). No respondent could describe or show
The top-ranked Poisson generalized linear models us any feeding sign by sun bears.
(ΔAICc , ) for encounters with small wildlife contained Respondents considered nine species to be destructive to
the predictors age, immature palms, border and time the oil palm crop but there was considerable variation
(Table ). For large mammals, top-ranked models among these in terms of perceived destructiveness (Fig. ).
(ΔAICc , ) contained the same predictors, along with ma- Compared to macaques, pigs and elephants, sun bears
ture palms (Table ). Overdispersion parameters for all caused little damage (Table S). Model selection for the bi-
models were , ., supporting use of the Poisson distribu- nomial generalized linear models identified top-ranked
tion. Generalized variance inflation factor values were , , models that all contained palm shoots as a predictor of de-
indicating that multicollinearity between predictors was not structive behaviour (ΔAICc , ; Table ). Other variables
significant. Residuals versus fitted plots displayed good fits. included in the top-ranked models were plantation type
The generalized linear mixed model for small wildlife failed and bunch. Generalized variance inflation factor values sug-
to converge, and there was no variation between the random gested that multicollinearity was not significant. Binned re-
components (SD = ) of the large mammal generalized lin- sidual versus fitted plots displayed a good fit. Area under the
ear mixed model. curve for all models was .–., indicating adequate pre-
Respondents (n = ) identified eight species (excluding dictive power. The binomial generalized linear mixed
squirrels and birds) that fed on loose palm fruits, four that model failed to converge.
fed on harvested fruit bunches, and eight that fed on fruits Eight species were considered to be dangerous (n = re-
still on the palm (Fig. ). Only one respondent reported sun spondents; Table ). Among these, clouded leopards and es-
bears depredating oil palm fruits, and said they climbed the tuarine crocodiles Crocodylus porosus were considered to be
palms to feed. Respondents identified another seven species most dangerous. Sun bears were perceived to be as danger-
that fed on palm shoots, including two respondents who ous as orang-utans. Respondents could recount only one
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
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https://doi.org/10.1017/S0030605317001089Sun bears in oil palm plantations 615
TABLE 2 Top-ranked models (ΔAICc , ) for small wildlife (small-bodied mammals and snakes) encountered by respondents from oil
palm plantations in the Lower Kinabatangan, Sabah, Malaysia (Fig. ), with number of parameters (k), log likelihood, Akaike’s information
criterion adjusted for small sample sizes (AICc), change in AICc (ΔAICc), and Akaike weight.
Model1 k Log likelihood AICc ΔAICc Akaike weight
Immature + Border + Age 4 −259.07 526.51 0.00 0.24
Immature + Mature + Border + Age2 5 −258.24 527.03 0.52 0.18
Immature + Type + Border + Age2 5 −258.56 527.67 1.16 0.13
Immature + Border + Age + Size2 5 −258.62 527.79 1.29 0.12
Immature + Border + Time 6 −257.55 527.88 1.37 0.12
Immature + Border 3 −260.85 527.93 1.42 0.12
Immature + Mature + Border2 4 −260.06 528.49 1.99 0.09
Intercept only 1 −270.34 542.71 16.21 0.00
Immature, oil palms , years of age; Mature, oil palms . years of age; Type, plantation type; Border, bordering intact forest; Age, respondent age; Size,
total planted area; Time, length of time respondent worked in plantation.
Models with an additional parameter within ΔAICc # of an otherwise similar better-ranked model were not considered to be competitive despite having
strong support. The extra parameter represents noise and thus does not necessarily infer biological significance.
TABLE 3 Top-ranked models (ΔAICc , ) for large mammals encountered by respondents from oil palm plantations in the Lower
Kinabatangan, Sabah, Malaysia (Fig. ), with number of parameters (k), log likelihood, Akaike’s information criterion adjusted for
small sample sizes (AICc), change in AICc (ΔAICc), and Akaike weight.
Model1 K Log likelihood AICc ΔAICc Akaike weight
Immature + Mature + Border + Age 5 −202.98 416.52 0.00 0.33
Immature + Border + Age 4 −204.27 416.91 0.39 0.27
Immature + Mature + Border + Age + Size2 6 −202.72 418.22 1.70 0.14
Immature + Mature + Age 4 −204.97 418.31 1.79 0.13
Immature + Type + Border + Age2 5 −203.98 418.51 1.99 0.12
Intercept only 1 −211.03 424.10 7.57 0.01
Immature, oil palms , years of age; Mature, oil palms . years of age; Type, plantation type; Border, bordering intact forest; Age, respondent age; Size,
total planted area.
Models with an additional parameter within ΔAICc # of an otherwise similar better-ranked model were not considered to be competitive despite having
strong support. The extra parameter represents noise and thus does not necessarily infer biological significance.
mauling by a clouded leopard and three by sun bears. Most plantations bordering forest, which probably serves as a ref-
respondents said they would retreat from a dangerous ani- uge (Rajaratnam et al., ; Nakashima et al., ); for ex-
mal (.%), but .% said they would sometimes chase the ample, although radio-collared sun bears ventured into oil
animal away. Very few admitted that they would capture palm plantations far (. km) from forest, they retreated to
(.%) or kill (.%) a dangerous animal. cover during daylight (Normua et al., ; Cheah, ).
Older respondents encountered more species, probably
because they had worked for longer at the plantation. We
Discussion found a positive association between years in a plantation
and the number of small wildlife species encountered.
Macaques and bearded pigs were the most commonly en- Elephants, porcupines Hystrix sp., macaques and
countered species, successfully utilizing the oil palm land- bearded pigs were all perceived to be particularly destructive
scape. Snakes, leopard cats and civets were also commonly of oil palm crops, in line with results from other studies
encountered, attracted by the abundance of rodent prey (Sabah Wildlife Department, ; Azhar et al., ;
(Rajaratnam et al., ). Sun bears, however, were rarely Luskin et al., ). These species fed on palm shoots, a
encountered, which suggests either avoidance of plantations strong indicator of destructive feeding. Young palms are
or elusive behaviour by the species. particularly at risk as the shoot is exposed and the palm eas-
Respondents from plantations containing immature oil ily destroyed. Sun bears also apparently fed on palm shoots,
palms encountered more species. Wildlife may be more vis- but rarely compared to other species (Fig. ). Feeding on
ible in these plantations, and the palms readily consumed. fruit bunches was also considered to be destructive.
Encounters with large mammals were associated with Bunches were mainly consumed by bearded pigs and maca-
palms of both age classes, suggesting that cover was attractive ques, both abundant and occurring in large groups. Ripe
to them. Respondents encountered more species in fruit bunches are destined for oil palm mills, making any
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
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https://doi.org/10.1017/S0030605317001089616 R. Guharajan et al.
FIG. 2 Records of wildlife species feeding on (a) loose fruits scattered on the ground, (b) harvested fruit bunches on the ground, (c)
fruits on the palm tree, and (d) oil palm shoots, as reported by respondents (n = ) from oil palm plantations in the Lower
Kinabatangan, Sabah, Malaysian Borneo (Fig. ).
human–wildlife conflict in Sabah (Sabah Wildlife
Department, ), and now also in adjacent Kalimantan,
Indonesia (Suba et al., ). Sun bears were considered to
be negligibly destructive but were often feared, although
only a few attacks were reported. In other parts of their
range, attacks by sun bears are reportedly more common
(Sethy & Chauhan, ).
We were surprised that respondents tended not to view
bears as being destructive to oil palms, as other studies
have found them to be destructive to many other crops, as
evidenced by conspicuous feeding sign and damage
(Fredriksson, ; Sethy & Chauhan, ; Scotson et al.,
FIG. 3 Wildlife species considered to be destructive to the oil
palm crop according to respondents (n = ) from oil palm ; Wong et al., ). We suspect that the bears fed largely
plantations in the Lower Kinabatangan, Sabah, Malaysian on loose fruits and fruit bunches (Plate ), which would cause
Borneo (Fig. ). little visible damage and leave no definitive evidence of their
presence (Fig. ). We knew of a sun bear feeding in a plan-
tation but we could not find any feeding sign; however, we
loss highly undesirable. Kebun respondents were more apt found abundant fresh sign (claw marks on trees) in neigh-
to perceive wildlife as being destructive, probably because bouring forest. Camera-trapped sun bears in forest adjacent
of their limited yield and lack of resources to mitigate to plantations were active mainly during crepuscular and
crop depredation. nocturnal hours, when human presence is minimal (R.
Three species ranked highly in terms of both destructive- Guharajan et al., unpubl. data), which explains why few re-
ness and danger: elephants, macaques and bearded pigs spondents saw them. Sun bears are known to become more
(Fig. ). Among these, elephants are at the forefront of nocturnal when feeding on crops (Normua et al., ; Sethy
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
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https://doi.org/10.1017/S0030605317001089Sun bears in oil palm plantations 617
TABLE 4 Top-ranked models for wildlife destructiveness in oil palm plantations in the Lower Kinabatangan, Sabah, Malaysia (Fig. ), with
number of parameters (k), log likelihood, Akaike’s information criterion adjusted for small sample sizes (AICc), change in AICc (ΔAICc),
and Akaike weight.
Model1 k Log likelihood AICc ΔAICc Akaike weight
Bunch + Type + Shoot 4 −137.11 282.40 0.00 0.24
Type + Shoot 3 −138.38 282.87 0.47 0.19
Bunch + Type + Mature + Shoot2 5 −136.88 284.04 1.63 0.10
Type + Mature + Shoot2 4 −138.00 284.20 1.79 0.10
Bunch + Type + Palm + Shoot2 5 −136.97 284.22 1.81 0.10
Bunch + Immature + Type + Shoot2 5 −136.97 284.22 1.82 0.10
Bunch + Shoot 3 −139.06 284.24 1.84 0.09
Bunch + Type + Loose + Shoot2 5 −137.03 284.34 1.93 0.09
Intercept only 1 −145.81 293.63 11.23 0.00
Loose, loose oil palm fruits; Bunch, harvested fruit bunches; Palm, fruits on the oil palm; Shoot, oil palm shoots; Mature, oil palms . years of age;
Immature, oil palms , years of age; Type, plantation type
Models with an additional parameter within ΔAICc # of an otherwise similar better-ranked model were not considered to be competitive despite having
strong support. The extra parameter represents noise and thus does not necessarily infer biological significance.
TABLE 5 Mean ± SD danger level ranks of wildlife species according
to respondents (n = ) from oil palm plantations in the Lower
Kinabatangan, Sabah, Malaysia (Fig. ), with the total number of
records and the number of records in which respondents were
able to rank the species.
No. of
Mean ± SD Total no. ranked
Species danger level rank1 of records records2
Macaque 1.90 (0.74) 14 10
Bearded pig 1.94 (0.77) 18 16
Bornean elephant 2.18 (0.8) 25 22
Sun bear 2.33 (1.15) 9 3
Bornean orang-utan 2.33 (0.71) 11 9
Snake 2.36 (0.68) 63 55
Estuarine crocodile 3.00 (0.00) 10 9
Sunda clouded 3.00 (0.00) 5 5 FIG. 4 Mean destructiveness and danger level ranks assigned to
leopard species by respondents from oil palm plantations in the Lower
Ranks: , least dangerous; , dangerous; , extremely dangerous. Kinabatangan, Sabah, Malaysian Borneo (Fig. ). Civets and
This number was used in the calculation of the mean danger level rank. porcupines have a mean danger level rank of , as no respondent
reported them as being dangerous.
& Chauhan, ; Wong et al., ); for example, sun bears it. However, discoveries of butchered sun bears (L. Liman,
fitted with global positioning system collars in Krau Wildlife WWF-Malaysia, pers. comm.) suggest that targeted poach-
Reserve, Peninsular Malaysia, made frequent night-time in- ing may occur, although the scale is unclear.
cursions into adjacent oil palm plantations (Cheah, ). It is likely that sun bears benefit nutritionally from eating
We presumed that oil palm plantations not only reduced oil palm fruits, especially in inter-mast years when fruits are
the area of natural forest but also increased the mortality risk scare in the forest, and insects alone are insufficient (Wong
to bears. We could not discern whether bears were subject to et al., ; Fredriksson et al., ). Camera traps in our
increased mortality; however, respondents’ perceptions sug- study area indicated that sun bears were in good physical
gest that bears are not a target of retribution. They may still condition (R. Guharajan, unpubl. data), suggesting that
be killed opportunistically but this would occur rarely, given they were supplementing their diet from plantations. In
that they are rarely seen. Mortality may also occur from by- Peninsular Malaysia, bears that routinely fed in oil palm
catch: sun bears at a forest–oil palm interface in Peninsular plantations were some of the heaviest recorded from the
Malaysia had a high incidence of injuries from snares set for wild (Cheah, ). Such feeding entails risks; however, un-
ungulates (Cheah, ). We did not find evidence of this like the destructive feeding of bears on other crops, sun
from camera-trap photographs in our study area (R. bears can feed on oil palm fruits without causing damage.
Guharajan et al., unpubl. data), nor did respondents report This behaviour, combined with mainly nocturnal, solitary
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
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https://doi.org/10.1017/S0030605317001089618 R. Guharajan et al.
A N C R E N A Z , M., O R A M , F., A M B U , L., L AC K M A N , I., A H M A D , E.,
E L A H A N , H. et al. () Of Pongo, palms and perceptions: a
multidisciplinary assessment of Bornean orang-utans Pongo
pygmaeus in an oil palm context. Oryx, , –.
A R N O L D , T.W. () Uninformative parameters and model selection
using Akaike’s information criterion. The Journal of Wildlife
Management, , –.
A U G E R I , D.M. () On the biogeographic ecology of the Malayan sun
bear. PhD thesis. University of Cambridge, Cambridge, UK.
A Z H A R , B., L I N D E N M AY E R , D.B., W O O D , J., F I S C H E R , J. & Z A K A R I A ,
M. () Ecological impacts of oil palm agriculture on forest
mammals in plantation estates and smallholdings. Biodiversity and
Conservation, , –.
A Z M I , R. () Natural Vegetation of the Lower Kinabatangan.
Unpublished report. WWF-Malaysia and Sabah Forestry
Department, Kota Kinabalu, Malaysia.
C A M P B E L L -S M I T H , G., C A M P B E L L -S M I T H , M., S I N G L E T O N , I. &
PLATE 1 A typical forest–oil palm interface in the Lower L I N K I E , M. () Apes in space: saving an imperilled orangutan
Kinabatangan, Sabah, Malaysian Borneo (Fig. ). Sun bears population in Sumatra. PLoS ONE, (), e.
Helarctos malayanus can easily pass under electric fences (on the C H E A H , C.P.I. () The ecology of Malayan sun bears (Helarctos
left) designed to keep elephants Elephas maximus borneensis out malayanus) at the Krau Wildlife Reserve, Pahang, Malaysia and
of plantations, and feed on the abundant loose fruits and fruit adjacent plantations. PhD thesis. Universiti Putra Malaysia,
bunches on the ground. Selangor, Malaysia.
E S T E S , J.G., O T H M A N , N., I S M A I L , S., A N C R E N A Z , M., G O O S S E N S , B.,
A M B U , L.N. et al. () Quantity and configuration of available
feeding, increases the ability of sun bears to persist in this
elephant habitat and related conservation concerns in the Lower
landscape. However, we do not suggest that the loss of Kinabatangan floodplain of Sabah, Malaysia. PLoS ONE, (),
cover and fruit and insect diversity, components of natural e.
forest that are used and presumably needed by sun bears, is F R E D R I K S S O N , G.M. () Human–sun bear conflicts in East
compensated for by accessing oil palm fruits. Kalimantan, Indonesian Borneo. Ursus, , –.
F R E D R I K S S O N , G.M., D A N I E L S E N , L.S. & S W E N S O N , J.E. ()
Impacts of El Niño related drought and forest fires on sun bear fruit
Acknowledgements resources in lowland dipterocarp forest of East Borneo. Biodiversity
and Conservation, , –.
We thank the Sabah Biodiversity Centre and Sabah Wildlife F R E D R I K S S O N , G.M., S T E I N M E T Z , R., W O N G , S. & G A R S H E L I S , D.L.
(IUCN SSC B E A R S P E C I A L I S T G R O U P ) () Helarctos
Department for their support; and Lorraine Scotson and
malayanus. In The IUCN Red List of Threatened Species : e.
N. Guharajan for comments on interview design. We TA. Http://dx.doi.org/./IUCN.UK..RLTS.
thank all staff of FGV-Pontian United Plantations, TA.en [accessed July ].
Gomantong, Linddale and Sungai Pin estates, as well as re- F R E D R I K S S O N , G.M., W I C H , S.A. & T R I S N O () Frugivory
sidents of Kg. Menggaris, Kg. Batu Putih, and Kg. in sun bears (Helarctos malayanus) is linked to El
Perpaduan Datuk Moh. Funding was provided by the Niño-related fluctuations in fruiting phenology, East
Kalimantan, Indonesia. Biological Journal of the Linnean Society,
Association of Zoos and Aquariums, Columbus Zoo and , –.
Aquarium, Hauser Bears, the International Association for K O H , L.P. & W I L C O V E , D.S. () Is oil palm agriculture
Bear Research and Management, Bell Museum of Natural really destroying tropical biodiversity? Conservation Letters,
History, and Wildlife Reserves Singapore. , –.
L I U , F., M C S H E A , W.J., G A R S H E L I S , D.L., Z H U , X., W A N G , D. &
S H A O , L. () Human–wildlife conflicts influence attitudes but not
Author contributions necessarily behaviors: factors driving the poaching of bears in
China. Biological Conservation, , –.
RG, BG, STW and DLG conceived the project. RG and L U S K I N , M.S., C H R I S T I N A , E.D., K E L L E Y , L.C. & P O T T S , M.D. ()
MAM collected the data. RG analysed the data. RG and Modern hunting practices and wild meat trade in the oil palm
plantation-dominated landscapes of Sumatra, Indonesia. Human
DLG wrote the article, with editing by NKA and BG. Ecology, , –.
SKSSN assisted with the permits. M A R C H A L , V. & H I L L , C. () Primate crop-raiding: a study of local
perceptions in four villages in North Sumatra, Indonesia. Primate
Conservation, , –.
References M E I J A A R D , E., B U C H O R I , D., H A D I P R A K A R S A , Y., U TA M I -A T M O KO , S.
S., N U R C A H YO , A., T J I U , A. et al. () Quantifying killing of
A B R A M , N.K., X O F I S , P., T Z A N O P O U LO S , J., M AC M I L L A N , D.C., orangutans and human–orangutan conflict in Kalimantan,
A N C R E N A Z , M., C H U N G , R. et al. () Synergies for improving oil Indonesia. PLoS ONE, (), e.
palm production and forest conservation in floodplain landscapes. N A K A S H I M A , Y., N A K A B AY A S H I , M. & S U KO R , J.A. () Space use,
PLoS ONE, (), e. habitat selection, and day-beds of the common palm civet
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 07 Feb 2022 at 04:20:16, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.1017/S0030605317001089Sun bears in oil palm plantations 619
(Paradoxurus hermaphroditus) in human-modified habitats in fas.usda.gov/data/oilseeds-world-markets-and-trade [accessed
Sabah, Borneo. Journal of Mammalogy, , –. July ].
N O R M U A , F., H I G A S H I , S., A M B U , L. & M O H A M E D , M. () Notes V I J AY , V., P I M M , S.L., J E N K I N S , C.N. & S M I T H , S.J. () The impacts
on oil palm plantation use and seasonal spatial relationships of sun of oil palm on recent deforestation and biodiversity loss. PLoS ONE,
bears in Sabah, Malaysia. Ursus, , –. (), e.
R D E V E LO P M E N T C O R E T E A M () R: A Language and Environment W O N G , S.T., S E R V H E E N , C., A M B U , L. & N O R H AY AT I , A. ()
for Statistical Computing. R Foundation for Statistical Computing, Impacts of fruit production cycles on Malayan sun bears and
Vienna, Austria. bearded pigs in lowland tropical forest of Sabah, Malaysian Borneo.
RAJARATNAM, R., S U N Q U I S T , M., R A J A R AT N A M , L. & A M B U , L. Journal of Tropical Ecology, , –.
() Diet and habitat selection of the leopard cat W O N G , W.-M., L E A D E R -W I L L I A M S , N. & L I N K I E , M. () Managing
(Prionailurus bengalensis borneoensis) in an agricultural landscape human–sun bear conflict in Sumatran agroforest systems. Human
in Sabah, Malaysian Borneo. Journal of Tropical Ecology, , Ecology, , –.
–. WWF-M A L A Y S I A () Bersatu Memerangi Pemburuan Haram
S A B A H W I L D L I F E D E P A R T M E N T () Sabah Wildlife Conservation (Working Together to Fight Poaching). WWF-Malaysia, Sabah,
Enactment . Kota Kinabalu, Sabah, Malaysia. Malaysia.
S A B A H W I L D L I F E D E P A R T M E N T () Elephant Action Plan. Kota Y U E , S., B R O D I E , J.F., Z I P K I N , E.F. & B E R N A R D , H. () Oil palm
Kinabalu, Sabah, Malaysia. plantations fail to support mammal diversity. Ecological
S C OT S O N , L., V A N N AC H O M C H A N , K. & S H A R P , T. () More Applications, , –.
valuable dead than deterred? Crop-raiding bears in Lao PDR.
Wildlife Society Bulletin, , –.
S E T H Y , J. & C H A U H A N , N.P.S. () Human–sun bears conflict in Biographical sketches
Mizoram, North East India: impact and conservation management.
International Journal of Conservation Science, , –. RO S H A N GU H A R A J A N and MO H D AZ Z U M A R MA G G U N A are inter-
S U B A , R.B., VA N D E R P LO E G , J., VA N ’ T Z E L F D E , M. , L A U , Y.W., ested in practical research and conservation initiatives. NI C O L A
W I S S I N G H , T.F., K U S T I AWA N , W. et al. () Rapid expansion of oil AB R A M promotes effective land-use planning in oil palm–forest land-
palm is leading to human–elephant conflicts in North Kalimantan scapes. BE N O Î T GO O S S E N S studies biodiversity responses to habitat
province of Indonesia. Tropical Conservation Science, , https://doi. fragmentation and degradation. SI E W TE WO N G works on sun bear con-
org/./. servation through holistic approaches. SE N T H I L V E L K.S.S. NA T H A N
U.S. D E P A R T M E N T O F A G R I C U LT U R E , F O R E I G N A G R I C U LT U R A L oversees wildlife management in Sabah. DA V I D L. GA R S H E L I S facilitates
S E R V I C E () Oilseeds: World Markets and Trade. Https://www. bear research and conservation worldwide.
Oryx, 2019, 53(4), 611–619 © 2017 Fauna & Flora International doi:10.1017/S0030605317001089
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 07 Feb 2022 at 04:20:16, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
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